Chapter 7. Ethical and Scientific Pitfalls Concerning Laboratory Research with Non-Human
7. Conclusions
137
those described above with dogs. Some NHPs species are particularly harmless and cooperative (e.g., marmosets or capuchin monkeys). Individuals from those species who are held captive for other reasons (e.g., rescued animals living in sanctuaries) could also be enrolled in experiments similar to the ones conducted by Bern and colleagues on dogs [140–143]. Even potentially dangerous NHPs, such as chimpanzees, can participate in experiments consensually, in the same way human participants do [41].
138
Acknowledgments: We wish to express our gratitude to the editor and anonymous referees for their detailed comments that greatly helped us improve the quality of the manuscript.
Conflicts of Interest: The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; the writing of the manuscript, or the decision to publish the results.
References
1. Phillips, K.A.; Bales, K.L.; Capitanio, J.P.; Conley, A.; Czoty, P.W.; ´t Hart, B.A.;
Hopkins, W.; Hopkins, W.D.; Hu, S.L.; et al. Why primate models matter. Am. J.
Primatol. 2014, 76, 801–827. [CrossRef] [PubMed]
2. Maestripieri, D. The Past, Present, and Future of Primate Psychology. In Primate Psychology; Maestripieri, D., Ed.; Harvard University Press: Cambridge, MA, USA, 2003; pp. 1–16.
3. European Commission. Seventh Report on the Statistics on the Number of Animals used for Experimental and other Scientific Purposes in the Member States of the European Union. Available online: http://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX:
52013DC0859 (accessed on 23 March 2017).
4. Lankau, E.W.; Turner, P.V.; Mullan, R.J.; Galland, G.G. Use of nonhuman primates in research in North America. J. Am. Assoc. Lab. Anim. Sci. 2014, 53, 278–282. [PubMed]
5. Zhang, X.L.; Pang, W.; Hu, X.T.; Li, J.L.; Yao, Y.G.; Zheng, Y.T. Experimental primates and non-human primate (NHP) models of human diseases in China: Current status and progress. Zool. Res. 2014, 35, 447–464. [PubMed]
6. Zhou, Q. Balancing the welfare: The use of non-human primates in research. Trends Gen.
2014, 30, 476–478. [CrossRef] [PubMed]
7. Friedman, H.; Haigwood, N.; Ator, N.; Newsome, W.; Allan, J.S.; Golos, T.G.;
Kordower, J.H.; Shade, R.E.; Goldberg, M.E.; Bailey, M.R.; et al. The Critical Role of Nonhuman Primates in Medical Research-White Paper. Pathog. Immun. 2017, 2, 352–
365. [CrossRef] [PubMed]
8. Sanal, M.G. Future of liver transplantation: Non-human primates for patient-specific organs from induced pluripotent stem cells. World J. Gastroenterol 2011, 17, 3684–
3690. [CrossRef] [PubMed]
9. Knight, A. The poor contribution of chimpanzee experiments to biomedical progress. J.
Appl. Anim. Welf. Sci. 2007, 10, 281–308. [CrossRef]
139
10. Bailey, J. An assessment of the role of chimpanzees in AIDS vaccine research. ATLA 2008, 36, 381–428.
11. Thew, M. Primate studies: Trials don’t always translate. Nature 2012, 484, 167.
[CrossRef]
12. Bailey, J.; Taylor, K. Non-human primates in neuroscience research: The case against its scientific necessity. ATLA 2016, 44, 43–69.
13. Harlow, H.F. The nature of love. Am. Psychol. 1958, 13, 673–685. [CrossRef]
14. Selemon, L.D.; Goldman-Rakic, P.S. Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci. 1985, 5, 776–794.
[CrossRef] [PubMed]
15. Lewontin, R.C. Primate Models of Human Traits. In Aping Science: A Critical Analysis of Research at the Yerkes Regional Primate Research Center; Committee on Animal Models in Biomedical Research, Ed.; Medical Research Modernization Committee: New York, NY, USA, 1995; pp. 5–24.
16. Goodall, J. Tool-using and aimed throwing in a community of free-living chimpanzees.
Nature 1964, 201, 1264–1266. [CrossRef]
17. Liu, Q.; Fragaszy, D.M.; Visalberghi, E. Wild capuchin monkeys spontaneously adjust actions when using hammer stones of different mass to crack nuts of different resistance.
Am. J. Phys. Anthrop. 2016, 161, 53–61. [CrossRef]
18. Kawamura, S. The process of sub-culture propagation among Japanese macaques.
Primates 1959, 2, 43–60. [CrossRef]
19. Eshchar, Y.; Izar, P.; Visalberghi, E.; Resende, B.; Fragaszy, D. When and where to practice: Social influences on the development of nut-cracking in bearded capuchins (Sapajuslibidinosus). Anim. Cogn. 2016, 19, 605–618. [CrossRef] [PubMed]
20. Gallup, G.G., Jr. Chimpanzees: Self-recognition. Science 1970, 167, 86–87. [CrossRef]
21. Toda, K.; Platt, M.L. Animal cognition: Monkeys pass the mirror test. Curr. Biol. 2015, 25, 64–66. [CrossRef]
22. Freeman, H.D.; Gosling, S.D. Personality in nonhuman primates: A review and evaluation of past research. Am. J. Primatol. 2010, 72, 653–671. [CrossRef]
23. Cheney, D.; Seyfarth, R.; Smuts, B. Social relationships and social cognition in nonhuman primates. Science 1986, 234, 1361–1366. [CrossRef]
24. Roubová, V.; Koneˇcná, M.; Šmilauer, P.; Wallner, B. Whom to groom and for what?
Patterns of grooming in female Barbary macaques (Macaca sylvanus). PLoS ONE 2015, 10, e0117298. [CrossRef] [PubMed]
140
25. Smuts, B.B.; Cheney, D.L.; Seyfarth, R.M.; Wrangham, R.W. Primate Societies;
University of Chicago Press: Chicago, IL, USA, 2008.
26. Sterck, E.H.; Goossens, B.M. The meaning of “macaque” facial expressions. Proc. Natl.
Acad. Sci. USA 2008, 105, E71. [CrossRef]
27. Goodall, J. The Chimpanzees of Gombe: Patterns of Behavior; Harvard University Press:
Cambridge, MA, USA, 1986.
28. De Waal, F.B. Putting the altruism back into altruism: The evolution of empathy. Ann.
Rev. Psychol. 2008, 59, 279–300. [CrossRef] [PubMed]
29. Yang, B.; Anderson, J.R.; Li, B.G. Tending a dying adult in a wild multi-level primate society. Curr. Biol. 2016, 26, 403–404. [CrossRef] [PubMed]
30. Brosnan, S.; De Waal, F.B. Monkeys reject unequal pay. Nature 2003, 425, 297–299.
[CrossRef] [PubMed]
31. Wheeler, B.C. Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp resources from conspecifics. Proc. Biol. Sci. 2009, 276, 3013–3018. [CrossRef]
[PubMed]
32. Bard, K.A.; Gaspar, A.D.; Vick, S.J. Chimpanzee faces under the magnifying glass:
Emerging methods reveal cross-species similarities and individuality. In Personality and Temperament in Nonhuman Primates; Weiss, A., King, J.E., Murray, L., Eds.; Springer:
New York, NY, USA, 2011; pp. 193–231.
33. Hobaiter, C.; Byrne, R.W. The gestural repertoire of the wild chimpanzee. Anim. Cogn.
2011, 14, 745–767. [CrossRef]
34. Gaspar, A.; Esteves, F.; Arriaga, P. On prototypical facial expressions versus variation in facial behavior: What have we learned on the “visibility” of emotions from measuring facial actions in humans and apes. In The Evolution of Social Communication in Primates; Pina, M., Gontier, N., Eds.; Springer International Publishing: Heidelberg, Germany, 2014; pp. 101–126.
35. Pasquaretta, C.; Levé, M.; Claidière, N.; Van De Waal, F.; Whiten, A.; MacIntosh, A.J.;
Pelé, M.; Bergstrom, M.L.; Borgeaud, C.; Brosnan, S.F.; et al. Social networks in primates: Smart and tolerant species have more efficient networks. Sci. Rep. 2014, 4, 7600. [CrossRef]
36. Gardner, R.A.; Gardner, B.T. Teaching sign language to a chimpanzee. Science 1969, 165, 664–672. [CrossRef]
37. Patterson, F.G. The gestures of a gorilla: Language acquisition in another pongid. Brain Lang 1978, 5, 72–97. [CrossRef]
141
38. Matsuzawa, T.; Hasegawa, Y.; Gotoh, S.; Wada, K. One-trial long-lasting food-aversion learning in wild Japanese monkeys (Macaca fuscata). Behav. Neural Biol. 1983, 39, 155–159. [CrossRef]
39. Amici, F.; Barney, B.; Johnson, V.E.; Call, J.; Aureli, F. A modular mind? A test using individual data from seven primate species. PLoS ONE 2012, 7, e51918. [CrossRef]
40. Cantlon, J.F.; Brannon, E.M. Basic math in monkeys and college students. PLoS Biol.
2007, 5, e328. [CrossRef] [PubMed]
41. Inoue, S.; Matsuzawa, T. Working memory of numerals in chimpanzees. Curr. Biol.
2007, 17, 1004–1005. [CrossRef] [PubMed]
42. Natale, F.; Antinucci, F.; Spinozzi, G.; Potí, P. Stage 6 object concept in nonhuman primate cognition: A comparison between gorilla (Gorilla gorilla gorilla) and Japanese macaque (Macaca fuscata). J. Comp. Psychol. 1986, 100, 335–339. [CrossRef]
43. Herrmann, E.; Call, J. Are there geniuses among the apes? Phil. Trans. R. Soc. B. 2012, 367, 2753–2761. [CrossRef] [PubMed]
44. Drucker, C.B.; Brannon, E.M. Rhesus monkeys (Macaca mulatta) map number onto space. Cognition 2014, 132, 57–67. [CrossRef] [PubMed]
45. Fenton, A. On the need to redress an inadequacy in animal welfare science: Toward an internally coherent framework. Biol. Phil. 2012, 27, 73–93. [CrossRef]
46. Wendler, D. Should protections for research with humans who cannot consent apply to research with nonhuman primates? Theor. Med. Bioeth. 2014, 35, 157–173. [CrossRef]
47. Conlee, K.M.; Rowan, A.N. The case for phasing out experiments on primates. Hastings Cent. Rep. 2012, 46, 20–26. [CrossRef] [PubMed]
48. European Commission. Special Eurobarometer: Science and Technology Report.
Available online: http://ec.europa.eu/commfrontoffice/publicopinion/archives/ebs/ebs_
340_en.pdf (accessed on 31 March 2017).
49. Price, N.; Bourne, J.; Rosa, M. Animal research: Australians rush to reject primate bill.
Nature 2016, 531, 35. [CrossRef] [PubMed]
50. Harding, J.D. Nonhuman Primates and Translational Research: Progress, Opportunities, and Challenges. ILAR J. 2017, 58, 141–150. [CrossRef]
51. Pollard, K.C. What Makes Us Human? Sci. Am. 2009, 300, 32–37. [CrossRef]
52. Jin, H.; Liu, L.; Ding, H.; He, M.; Zhang, C.; Zhong, X. Comparison of femtosecond laser-assisted corneal intrastromal xenotransplantation and the allotransplantation in rhesus monkeys. BMC Ophthalmol. 2017, 17, 202. [CrossRef] [PubMed]
142
53. He, M.; Jin, H.; He, H.; Ding, H.; Wang, W.; Liu, L.; Zhang, C.; Zhong, X. Femtosecond Laser-Assisted Small Incision Endokeratophakia Using a Xenogeneic Lenticule in Rhesus Monkeys. Cornea 2018, 37, 354–361. [CrossRef] [PubMed]
54. Bilz, K.; Nadler, J. Law, psychology, and morality. In Psychology of Learning and Motivation: Moral Judgment and Decision Making; Medin, D., Skitka, L., Bartels, D., Bauman, C., Eds.; Academic Press: San Diego, CA, USA, 2009; Volume 50, pp. 101–
124.
55. Barnes, E. Diseases and Human Evolution; University of New Mexico Press:
Albuquerque, NM, USA, 2007.
56. Mandal, J.; Acharya, S.; Parija, S.C. Ethics in human research. Trop. Parasitol. 2011, 1, 2–57. [PubMed]
57. Council for International Organizations of Medical Sciences. International ethical guidelines for biomedical research involving human subjects. Bull. Med. Ethics 2002, 182, 17–23.
58. Beauchamp, T.L.; Childress, J.F. Principles of Biomedical Ethics, 4th ed.; Oxford University Press: New York, NY, USA, 2005.
59. Canli, T. Neurogenethics: An emerging discipline at the intersection of ethics, neuroscience, and genomics. Appl. Transl. Genom. 2015, 5, 18–22. [CrossRef]
60. Smith, C.U.C. Confronting ethical permissibility in animal research: Rejecting a common assumption and extending a principle of justice. Theor. Med. Bioeth. 2014, 35, 175–185. [CrossRef]
61. Miracle, V.A. The Belmont report: The triple crown of research ethics. Dimens. Crit.
Care Nurs. 2016, 35, 223–228. [CrossRef]
62. Nardini, C. The ethics of clinical trials. Ecancermedicalscience 2014, 8, 387. [PubMed]
63. Gluck, J.P. Moving beyond the welfare standard of psychological well-being for nonhuman primates: The case of chimpanzees. Theor. Med. Bioeth. 2014, 35, 105–116.
[CrossRef] [PubMed]
64. Jones, R.C.; Greek, R. A review of the Institute of Medicine’s analysis of using chimpanzees in biomedical research. Sci. Eng. Ethics 2014, 20, 481–504. [CrossRef]
[PubMed]
65. Thomas, D. Laboratory animals and the art of empathy. J. Med. Ethics 2005, 31, 197–
202. [CrossRef] [PubMed]
66. Lowenstein, P.R. Clinical trials in gene therapy: Ethics of informed consent and the future of experimental medicine. Curr. Opin. Mol. Ther 2008, 10, 428–430.
143
67. Ollson, I.A.S.; Sandøe, P. “What’s wrong with my monkey?” Ethical perspectives on germline transgenesis in marmosets. Transgenic Res. 2010, 19, 181–186. [CrossRef]
[PubMed]
68. Kant, I. Lectures on Ethics (First Published 1775); Hackett Publishing Co.: Indianapolis, IN, USA, 1930.
69. Kant, I. Groundwork of the Metaphysic of Morals (First Published 1785); Hutchinson University Library: Hutchinson, KA, USA, 1972.
70. Darwall, S. Deontology; Blackwell Publishing: Oxford, MA, USA, 2002.
71. Barrow, J.M.; Gossman, W.G. Deontology; StatPearls Publishing: Treasure Island, FL, USA, 2017. Available online: https://www.ncbi.nlm.nih.gov/books/NBK459296/
(accessed on 11 March 2018).
72. Ross, W.D. The Right and the Good; Clarendon Press: Oxford, NY, USA, 1930.
73. Regan, T. The Case for Animal Rights; University of California Press: Berkeley, CA, USA, 1983.
74. Council for International Organizations of Medical Sciences. International Guiding Principles for Biomedical Research Involving Animals. Available online:
https://grants.nih.gov/grants/olaw/Guiding_Principles_ 2012.pdf (accessed on 23 March 2017).
75. European Parliament. Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the Protection of Animals Used for Scientific purposes Text with EEA Relevance. Available online: http://eur-lex.europa.eu/legal-content/EN/
TXT/?uri=CELEX:32010L0063 (accessed on 11 March 2018).
76. Ferdowsian, H. Human and animal research guidelines: Aligning ethical constructs with new scientific developments. Bioethics 2011, 25, 472–478. [CrossRef]
77. Ferdowsian, H.; Fuentes, A. Harms and deprivation of benefits for nonhuman primates in research. Theor. Med. Bioeth. 2014, 35, 143–156. [CrossRef] [PubMed]
78. Lepola, P.; Needham, A.; Mendum, J.; Sallabank, P.; Neubauer, D.; de Wildt, S.
Informed consent for paediatric clinical trials in Europe. Arch. Dis. Child. 2016, 101, 1017–1025. [CrossRef] [PubMed]
79. Kelley, M.C.; Brazg, T.; Wilfond, B.S.; Lengua, L.J.; Rivin, B.E.; Martin-Herz, S.P.;
Diekema, D.S. Ethical challenges in research with orphans and vulnerable children: A qualitative study of researcher experiences. Int. Health 2016, 8, 187–196. [CrossRef]
144
80. Lit, L.; Schweitzer, J.B.; Iosif, A.M.; Oberbauer, A.M. Owner reports of attention, activity, and impulsivity in dogs: A replication study. Behav. Brain Funct. 2010, 6, 1.
[CrossRef] [PubMed]
81. Sauer, U.; Phillips, B.; Reid, K.; Schmit, V.; Jennings, M. Ethical review of projects involving non-human primates funded under the European Union’s 7th Research Framework Programme. ATLA 2013, 41, 271–306. [PubMed]
82. Glander, K.E.; Fedigan, L.M.; Fedigan, L.; Chapman, C. Field methods for capture and measurement of three monkey species in Costa Rica. Folia Primatol. 1991, 57, 70–82.
[CrossRef] [PubMed]
83. Cunningham, E.P.; Unwin, S.; Setchell, J.M. Darting Primates in the Field: A Review of Reporting Trends and a Survey of Practices and Their Effect on the Primates Involved.
Int. J. Primatol. 2015, 36, 911–932. [CrossRef]
84. Unwin, S.; Ancrenaz, M.; Mahe, S.; Boardman, W. African primate handling and anaesthesia. In Pan African Sanctuary Alliance Veterinary Health Manual, 2nd ed.;
Unwin, S.M., Cress, D., Colin, C., Bailey, W., Boardman, W., Eds.; Pan African Sanctuary Alliance: Portland, OR, USA, 2009; pp. 214–287.
85. Bentham, J. The Principles of Morals and Legislation (First Published 1789);
Prometheus Books: New York, NY, USA, 1988.
86. Mill, J.S. Utilitarianism; Parker; Son & Bourn: London, UK, 1863.
87. Singer, P. Practical Ethics; Cambridge University Press: Cambridge, UK, 1979.
88. Bayne, K.; Morris, T. Laws, regulations and policies relating to the care and use of nonhuman primates in biomedical research. In Nonhuman Primates in Biomedical Research: Biology and Management; Abee, C.R., Mansfield, K., Tardif, S.D., Morris, T., Eds.; Academic Press: Oxford, MA, USA, 2012; pp. 35–56.
89. Garner, P. The Significance of Meaning: Why Do Over 90% of Behavioral Neuroscience Results Fail to Translate to Humans, and What Can We Do to Fix It? ILAR J. 2014, 55, 438–456. [CrossRef] [PubMed]
90. Food and Drug Administration. Innovation/Stagnation: Challenge and Opportunity on the Critical Path to New Medical Products. Available online: https://www.who.int/
intellectualproperty/documents/en/ FDAproposals.pdf (accessed on 23 March 2017).
91. Cummings, J.L.; Morstorf, T.; Zhong, K. Alzheimer’s disease drug-develop ment pipeline: Few candidates, frequent failures. Alzheimer’s Res. Ther. 2014, 6, 37.
[CrossRef]
145
92. Perrin, S. Preclinical research: Make mouse studies work. Nature 2014, 507, 423–425.
[CrossRef]
93. VandeBerg, J.L.; Zola, S.M. A unique biomedical resource at risk. Nature 2005, 437, 30–
32. [CrossRef]
94. Wolf, D.P. The non-human primate oocyte and embryo as a model for women, or is it vice versa? Theriogenology 2008, 69, 31–36. [CrossRef]
95. World Health Organization. Access to Medicine Index 2016. Available online:
http://accesstomedicineindex. org/media/atmi/Access-to-Medicine-Index-2016.pdf (accessed on 23 March 2017).
96. Ferdowsian, H.; Merskin, D. Parallels in sources of trauma, pain, distress, and suffering in humans and nonhuman animals. J Trauma Dis. 2012, 13, 448–468. [CrossRef]
97. Latham, N.R.; Mason, G.J. Maternal deprivation and the development of stereotypic behaviour. Appl. Anim. Behav. Sci 2008, 110, 84–108. [CrossRef]
98. Polanco, A. A Tinbergian review of self-injurious behaviors in laboratory rhesus macaques. Appl. Anim. Behav. Sci. 2016, 179, 1–10. [CrossRef]
99. Bentson, K.L.; Crockett, C.M.; Wahl, K.L.; Runeson, E.P.; Bellanca, R.U.; Lee, G.H.;
Thom, J.P.; Montgomery, H.B.; Yi, M.H.; McComas, J.G.; et al. Floating limb behaviors and self-biting are associated in laboratory monkeys. Am. J. Prim. 2010, 72, 725–733.
[CrossRef]
100. Bethell, E.J.; Holmes, A.; MacLarnon, A.; Semple, S. Emotion, evaluation and response slowing in a non-human primate: New directions for cognitive bias measures of animal emotion? Behav. Sci. 2016, 6, 2. [CrossRef] [PubMed]
101. Pryce, C.R.; Rüedi-Bettschen, D.; Dettling, A.C.; Feldon, J. Early life stress: Long-term physiological impact in rodents and primates. News Physiol. Sci. 2002, 17, 150–155.
[CrossRef] [PubMed]
102. Spinelli, S.; Chefer, S.; Suomi, S.J.; Higley, J.D.; Barr, C.S.; Stein, E. Early-life stress induces long-term morphologic changes in primate brain. Arch. Gen. Psychiatry 2009, 66, 658–665. [CrossRef] [PubMed]
103. Burrows, A.M. The facial expression musculature in primates and its evolutionary significance. Bioessays 2008, 30, 212–225. [CrossRef]
104. Gaspar, A. Comportamento facial em Pan e Homo. Ph.D. Thesis, Universidade Nova FCSH, Lisboa, Portugal, 2001.
105. Ekman, P.; Friesen, W.V. Facial Action Coding System: Manual; Consulting Psychologists Press: Palo Alto, CA, USA, 1978.
146
106. Vick, S.J.; Waller, B.M.; Parr, L.A.; Pasqualini, M.C.S.; Bard, K.A. A cross-species comparison of facial morphology and movement in humans and chimpanzees using the facial action coding system (FACS). J. Nonverbal. Behav. 2007, 31, 1–20. [CrossRef]
107. Parr, L.A.; Waller, B.M.; Burrows, A.M.; Gothard, K.M.; Vick, S.J. Brief communication: MaqFACS: A muscle-based facial movement coding system for the rhesus macaque. Am. J. Phys. Anthrop. 2010, 143, 625–630. [CrossRef]
108. Waller, B.M.; Lembeck, M.; Kuchenbuch, P.; Burrows, A.M.; Liebal, K. GibbonFACS:
A muscle-based facial movement coding system for hylobatids. Int. J. Primat. 2012, 33, 809–821. [CrossRef]
109. Caeiro, C.C.; Waller, B.M.; Zimmermann, E.; Burrows, A.M.; Davila-Ross, M.
OrangFACS: A muscle-based facial movement coding system for orangutans (Pongo spp.). Int. J. Primatol. 2013, 34, 115–129. [CrossRef]
110. Russell, W.; Burch, R. The Principles of Humane Experimental Technique; Methuen &
Co. Ltd.: London, UK, 1959.
111. Knight, A. The Costs and Benefits of Animal Experiments; Palgrave Macmillan:
Basingstoke, UK, 2011.
112. Wilson, S.L.; Ahearne, M.; Hopkinson, A. An overview of current techniques for ocular toxicity testing. Toxicology 2015, 327, 32–46. [CrossRef] [PubMed]
113. Ormandy, E.H.; Schuppli, C.A. Public attitudes toward animal research: A review.
Animals 2014, 4, 391–408. [CrossRef] [PubMed]
114. Plous, S. Attitudes toward the use of animals in psychological research and education:
Results from a national survey of psychology majors. Psychol. Sci. 1996, 7, 352–358.
[CrossRef]
116. Metzger, M.M. Knowledge of the animal welfare act and animal welfare regulations influences attitudes toward animal research. J. Am. Assoc. Lab. Anim. Sci. 2015, 54, 70–75. [PubMed]
117. Batson, C.D.; Duncan, B.D.; Ackerman, P.; Buckley, T.; Birch, K. Is empathic emotion a source of altruistic motivation? J. Pers. Soc. Psychol. 1981, 40, 290–302. [CrossRef]
118. Singer, P. The Most Good You Can Do: How Effective Altruism is Changing Ideas About Living Ethically; Yale University Press: New Haven, CT, USA, 2015.
119. Paul, E.S. Empathy with animals and with humans: Are they linked? Anthrozoös 2000, 13, 194–202. [CrossRef]
120. Davis, B.W.; Ostrander, E.A. Domestic dogs and cancer research: A breed-based genomics approach. ILAR J. 2014, 55, 59–68. [CrossRef]
147
121. Garner, J.P.; Gaskill, B.N.; Weber, E.M.; Ahloy-Dallaire, J.; Pritchett-Corning, K.R.
Introducing Therioepistemology: The study of how knowledge is gained from animal research. Lab. Anim. 2017, 46, 103–113. [CrossRef]
122. Peterson, D. Jane Goodall: The Woman who Redefined Man; Houghton Mifflin Harcourt:
Boston, MA, USA, 2014.
123. Brüne, M.; Brüne-Cohrs, U.; McGrew, W.C. Psychiatric treatment for great apes?
Science 2004, 306, 2039. [CrossRef]
124. Brüne, M.; Brüne-Cohrs, U.; McGrew, W.C.; Preuschoft, S. Psychopathology in great apes: Concepts, treatment options and possible homologies to human psychiatric disorders. Neurosci. Biobehav. Rev. 2006, 30, 1246–1259. [CrossRef] [PubMed]
125. Bradshaw, G.A.; Capaldo, T.; Lindner, L.; Grow, G. Building an inner sanctuary:
Complex PTSD in chimpanzees. J. Trauma Dis. 2008, 9, 9–34. [CrossRef]
126. Cibot, M.; Guillot, J.; Lafosse, S.; Bon, C.; Seguya, A.; Krief, S. Nodular worm infections in wild non-human primates and humans living in the Sebitoli area (Kibale National Park, Uganda): Do high spatial proximity favor zoonotic transmission? PLoS Negl. Trop. Dis. 2015, 9, e0004133. [CrossRef] [PubMed]
127. Lantz, E.L.; Lonsdorf, E.V.; Heintz, M.R.; Murray, C.M.; Lipende, I.; Travis, D.A.;
Santymire, R.M. Non-invasive quantification of immunoglobulin A in chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania. Am. J. Primatol. 2016, 80, e22558. [CrossRef] [PubMed]
128. Organisation for Economic Co-Operation and Development. Frascati Manual: Proposed Standard Practice for Surveys on Research and Experimental Development. Available online: https://www.oecd-ilibrary.org/science-and-technology/frascati-manual-2002_
9789264199040-en (accessed on 23 March 2017).
129. Kano, F.; Hirata, S.; Call, J. Social attention in the two species of pan: Bonobos make more eye contact than chimpanzees. PLoS ONE 2015, 10, e0129684. [CrossRef]
[PubMed]
130. Fröhlich, M.; Kuchenbuch, P.; Müller, G.; Fruth, B.; Furuichi, T.; Wittig, R.M.; Pika, S.
Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences. Sci. Rep. 2016, 6, 25887. [CrossRef] [PubMed]
131. Fujita, K.; Kuroshima, H.; Masuda, T. Do tufted capuchin monkeys (Cebusapella) spontaneously deceive opponents? A preliminary analysis of an experimental food-competition contest between monkeys. Anim. Cogn. 2002, 5, 19–25. [CrossRef]
[PubMed]
148
132. Pollick, A.S.; De Waal, F.B. Ape gestures and language evolution. Proc. Natl. Acad. Sci.
USA 2007, 104, 8184–8189. [CrossRef]
133. Fossey, D.; Harcourt, A.H. Feeding ecology of free-ranging mountain gorilla (Gorilla gorilla beringei). In Primate Ecology: Studies in Feeding and Ranging Behavior in Lemurs, Monkeys and Apes; Clutton-Brock, T.H., Ed.; Academic Press: New York, NY, USA, 1977; pp. 415–447.
134. Galdikas, B.M. Orangutan diet, range, and activity at Tanjung Puting, Central Borneo.
Int. J. Primatol. 1988, 9, 1–35. [CrossRef]
135. Kano, T. The Last Ape: Pygmy Chimpanzee Behavior and Ecology; Stanford University Press: Redwood City, CA, USA, 1992.
136. Chi, M.; Zhi-Pang, H.; Xiao-Fei, Z.; Li-Xiang, Z.; Wen-Mo, S.; Scott, M.B.; Xing-Wen, W.; Cui, L.-C.; Xiao, W. Distribution and conservation status of Rhinopithecusstrykeri in China. Primates 2014, 55, 377–382. [CrossRef]
137. Surbeck, M.; Hohmann, G. Primate hunting by bonobos at LuiKotale, Salonga National Park. Curr. Biol. 2008, 18, 906–907. [CrossRef] [PubMed]
138. Kühl, H.S.; Kalan, A.K.; Arandjelovic, M.; Aubert, F.; D’Auvergne, L.; Goedmakers, A.; Kühl, H.S.; Kalan, A.K.; Arandjelovic, M.; Aubert, F.; et al. Chimpanzee accumulative stone throwing. Sci. Rep. 2016, 6, 22219. [CrossRef] [PubMed]
139. Van Leeuwen, E.J.; Cronin, K.A.; Haun, D.B. Tool use for corpse cleaning in chimpanzees. Sci. Rep. 2017, 7, 44091. [CrossRef] [PubMed]
140. Rocha, S.; Gaspar, A.; Esteves, F. Developing children’s ability to recognize animal emotions—what does it take? A. study at the Zoo. HAIB 2016, 4, 59–79.
141. Berns, G.S.; Brooks, A.M.; Spivak, M. Functional MRI in awake unrestrained dogs.
PLoS ONE 2012, 7, e38027. [CrossRef]
142. Berns, G.S.; Brooks, A.M.; Spivak, M. Scent of the familiar: An fMRI study of canine brain responses to familiar and unfamiliar human and dog odors. Behav. Process 2015, 110, 37–46. [CrossRef]
143. Dilks, D.D.; Cook, P.; Weiller, S.K.; Berns, H.P.; Spivak, M.; Berns, G.S. Awake fMRI reveals a specialized region in dog temporal cortex for face processing. Peer J. 2015, 3, e1115. [CrossRef]
144. Cook, P.F.; Spivak, M.; Berns, G. Neurobehavioral evidence for individual differences in canine cognitive control: An awake fMRI study. Anim. Cogn. 2016, 19, 1–12.
[CrossRef]
149
145. Slater, H.; Milne, A.E.; Wilson, B.; Muers, R.S.; Balezeau, F.; Hunter, D.; Thiele, A.;
Griffiths, T.D.; Petkov, C.I. Individually customisable non-invasive head immobilisation system for non-human primates with an option for voluntary engagement. J. Neurosci.
Meth. 2016, 269, 46–60. [CrossRef]
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CHAPTER 8
Discussion
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